Coronavirus disease pandemic impact on emergency department visits for cardiovascular disease in Korea: A review

The coronavirus disease (COVID-19) pandemic has affected patient visits to the hospital, including visits to the emergency department (ED). This study aimed to analyze the impact of the COVID-19 pandemic on the patterns of ED visits and treatment in hospitals for diseases requiring urgent diagnosis and treatment. We analyzed entries from the South Korea National Emergency Department Information System claims database between January 1, 2018 and December 31, 2020. We analyzed data of patients who visited the ED with acute myocardial infarction (AMI), acute ischemic stroke (AIS), and acute hemorrhagic stroke (AHS). We found that the COVID-19 pandemic had impacted ED utilization and fatality in patients with AMI, AIS, and AHS.


Introduction
The first case of coronavirus disease (COVID- 19) was reported in Wuhan, China.Subsequently, the first case was reported in the Republic of Korea in January 2020 and has spread rapidly thereafter.On December 13, 2020, the number of confirmed cases in a day exceeded 1000 for the first time. [1]The Korea has experienced 3 waves of the COVID-19 pandemic in 2020, and the Korean government responded COVID-19 pandemic with a policy of three-level social distancing that upscaled or downscaled depending on the number of COVID-19 patients. [2]As the number of confirmed COVID-19 cases increased rapidly, older adults were waiting at home and were unable to receive proper treatment due to the lack of dedicated hospital beds. [2,3]he COVID-19 pandemic has affected patient visits to the hospital, including visits to the emergency department (ED).This trend was also previously observed for both the severe acute respiratory syndrome and Middle East respiratory syndrome. [4,5]Moreover, a study has shown that due to the COVID-19 pandemic, hospital visits of patients without COVID-19 during urgent medical situations decreased. [6]Some studies have investigated the impact of COVID-19 on acute illnesses; [7,8] however, only few were long-term nationwide studies.
Therefore, this study aimed to investigate the impact of the COVID-19 pandemic on the number of ED visits and fatality rate, as well as factors affecting fatality, in patients with acute myocardial infarction (AMI), acute ischemic stroke (AIS), and acute hemorrhagic stroke (AHS).

Study setting
The first case of COVID-19 in Korea was reported in January 2020; the number of cases has increased substantially thereafter.We defined 1 year from January 2020 as the main COVID-19 pandemic period and the 2 previous years (2018 and 2019) as the control period.We analyzed data of patients who visited the ED of the hospitals in Korea during the study period for the treatment of 3 major diseases, including AMI, AHS, and AIS.

Database and measurement variables
This study was a retrospective study that analyzed entries from the South Korea National Emergency Department Information System claims database between January 1, 2018 and December 31, 2020.The National Emergency Department Information System (NEDIS) database is a nationwide public database formed by the National Emergency Medical Center and contains all patient data who visited the ED of the hospitals in Korea.The database includes information on age, sex, region, disease onset time, ED arrival time, ED discharge time, ED visit route, ED discharge outcome, diagnosis codes according to the 10th revision of the International Classification of Diseases, and what medical services were used during stay in the ED.Three major diseases were defined based on the 10th revision of the International Classification of Diseases diagnostic code at discharge from the ED: AMI (I21-I22), AHS (I60-62), and AIS (I63-64).The outcomes were the number of ED visits, duration of symptom onset to ED arrival, length of ED stay, performance of emergency procedure, admission to the intensive care unit (ICU), and case fatality rate at the ED and hospital discharge.
Patients with AMI who underwent emergency procedures were defined as those who had undergone coronary angiography, percutaneous transluminal coronary angioplasty, stent insertion, thrombectomy, and off-pump coronary artery bypass surgery or with extracorporeal membrane oxygenation prescription code.Patients with AHS who underwent medical procedures were defined as those who had undergone craniotomy, craniectomy, burr hole, trephination, cerebral aneurysm clipping, and operation of cerebral arteriovenous malformation and embolization of cerebral aneurysm.Patients with AIS who underwent medical procedures were defined as those who had undergone intravenous thrombolysis, intra-arterial thrombolysis, extracranial percutaneous transluminal angioplasty or stent placement, and intracranial percutaneous transluminal angioplasty or stent placement.
All variables whose values were not entered, unknown, or missing were excluded.The duration of time to visit the ED after symptom onset and length of ED stay were calculated based on symptom onset time, ED visit time, and ED discharge time.The symptom onset of some patients was several months to several years before visiting the ED.To exclude chronic patients who could remarkably affect the statistics, the interquartile ranges were calculated, and the duration of ED visit after symptom onset exceeding the upper inner fences of the IQR (>Q3 + 1.5*IQR) was excluded.

Statistical analysis
All statistical analyses were performed using R version 4.1.0(R Foundation for Statistical Computing, Vienna, Austria).Descriptive statistics, categorical variables, and continuous variables are expressed as number, percentage, and mean and standard deviation, or median (interquartile range) according to whether normal distributions or not.respectively.The chisquared test was used to compare categorical variables between groups.Anderson-Darling normality test was performed to detect normality of continuous variables.Continuous variables without normality were statistically analyzed using the Mann-Whitney U test method between groups.Among the patients who visited the ED with AMI, AIS, and AHS, a multivariable logistic regression analysis was conducted to investigate associated factors with hospital death.Backward elimination method was used to select variables.Adjusted odds ratios and confidence intervals were calculated.Statistical significance was set at P < .05.A sensitivity analysis with the E-value to measure the robustness of the association between the COVID-19 pandemic and the outcomes for unmeasured or unadjusted confounding was performed.

Ethics statement
This study was approved by the Institutional Review Board of the Medicity Daegu (no.2020-10-001).The requirement of written informed consent was waived due to the retrospective nature of the study and use of anonymized data.

Results
On comparing the average number of patients visiting the ED for AMI, AIS, and AHS before and during the pandemic, we found a decreasing trend at -4.7%, -2.5%, and -2.7%, respectively, however, the number of patients who died at the hospital increased to 0.9%, 12.0%, and 7.5%, respectively (Fig. 1).
The median length from symptom onset to ED visit increased from 144.0 minutes to 151.0 minutes for AMI (P < .001)and from 229.5 minutes to 240.0 minutes for AIS (P < .001).The median length of ED stays slightly increased from 194.0 minutes to 199.0 minutes for AHS (P = .002)(Table 1).
The proportion of patients with AMI, AIS, and AHS who were referred by other hospitals showed a decreasing trend.Regarding the ED visit routes, the rate of visits through public emergency medical service (EMS) increased, while the rate of visits through private EMS used for transferring patients from another hospital decreased.After visiting the hospital, the rate of all major procedures increased; however, the ICU admission rate decreased.The rate of death in the ED and after visiting the ED increased from 8.3% to 8.8% for AMI (P = .015),from 3.5% to 4.0% for AIS (P < .001),and from 12.2% to 13.5% for AHS (P < .001)(Table 1).

Discussion
This is the first study that investigate the impact of the COVID-19 pandemic on ED visits among patients with cardiac and cerebrovascular problem who require prompt treatment during the COVID-19 pandemic.
The number of ED visits among patients with AMI, AIS and AHS significantly decreased since the outbreak of COVID-19 pandemic.Moreover, regarding ED visit routes, relative to the pre-pandemic period, the number of inter-hospital transfer and visits through private EMS decreased and use of 119 ambulances and self-visit increased.[11] A report from the United States showed that the number of ED visits decreased by 23% and 20% for heart attacks and strokes, respectively, in the 10 weeks following declaration of the COVID-19 national emergency. [12]A French study found that hospitalizations for patients with ST-segment elevation myocardial infarction were reduced by approximately 18% compared to those before the COVID-19 pandemic. [13]This might be attributed to a reduced total number of patients utilizing the ED.First, patients feared that contact with the health care system during hospital visits might increase their risk of contracting COVID-19.In a national survey conducted in April 2020, researchers found that >90% adults were concerned about contracting COVID-19 in the ED and that 29% adults responded that they avoided or delayed medical care because of anxiety of contracting COVID-19. [14]Second, due to patient's fear and confusion of their current symptoms as association with COVID-19, they might have underestimated the likelihood of a serious illness. [15]Last, there might be a decision not to burden the emergency medical system, which was already exposed to heavy workload and shortage of medial resources.In addition, policies such as social distancing and expansion of COVID-19 testing for screening could have caused a decrease in hospital use.
Other studies have suggested that low-level physical activity and serious work-related stress during lockdown as part of social policy may have contributed to lowering the incidence of AMI. [16,17]As the general ward and ED were closed due to confirmed COVID-19 cases and the number of patients showing symptoms of infection including fever and respiratory symptoms increased, the transfer between hospitals might have been limited.According to a local survey in Korea, EDs were repeatedly temporarily closed and an increase in medical staff undergoing self-quarantine was observed due to a surge in COVID-19 cases in February 2020. [18]oreover, we found that the time from symptom onset to visit to ED was delayed, and the time spent in the ED with AHS increased.There are several reasons for the delay in the time to ED visits.First, patients were reluctant to visit the hospital due to fear of COVID-19 transmission. [19,20]Second, the number of ambulances available for patients was insufficient.Since patients with suspected COVID-19 stayed and were transported using ambulance, it could be a potential source of the disease. [21]The use of ambulances might be restricted due to disinfection as it was used not only by confirmed patients but also by symptomatic individuals.According to some reports, the number of EMS calls increased rapidly during the COVID-19 pandemic, but the time required to answer calls was also increased significantly. [22,23]The turn-around time for confirming results of COVID-19 in acute-stage patients might have influenced the increase in the length of stay in the ED.As each hospital required confirmation of the COVID-19 test result as a system for admission, patients might have stayed longer in the ED until they were confirmed to be negative for COVID-19.
However, the rate of procedures including interventions such as coronary angiography and reperfusion increased compared to that before the pandemic.In addition, the rate of admission to the ICU decreased, and the fatality rate at the time of discharge from the ED and general ward increased.According to the European Society of Cardiology Guidelines, when ST-segment elevation myocardial infarction is diagnosed, immediate percutaneous coronary intervention is necessary because the fatality rate increases if treatment is delayed. [24]In stroke, hyper-acute treatment such as thrombolysis and thrombectomy also affects the neurological outcome and fatality of patients. [25]Although emergency procedures were performed, timely procedures could be delayed due to time delay after symptom onset, and the ED waiting time and admission rate to the ICU might have affected the fatality rate.
This study has several limitations.First, there is a lack of the detailed process for diagnosis and treatment using the NEDIS data compared with an in-depth review of hospital records.Second, as a limitation of the NEDIS data, there is a lack of analysis of factors other than those related to COVID-19 affecting ED visits, such as patient's classification systems, procedures, and hospitalization indications in each hospital.Third, there is a lack of the evaluation in the study about other factors that may affect the relationship between the variables.Last, an analysis of the direct impact of COVID-19 on each severe disease is lacking.

Conclusion
During the COVID-19 pandemic, the fatality rate of patients with cardiovascular diseases, such as AMI, AIS, and AHS, visiting the ED has increased.We hypothesized that the reduction of ED utilization due to the fear of contracting the disease, reduced capacity for transporting patients to the ED, increased difficulty in transporting patients to another hospital, increased length of ED stay, and decreased ICU admission after ED visit might have impacted the increase in fatality rate of patients with acute illnesses.To reduce fatality, effort should be made to improve these conditions.

Figure 1 .
Figure 1.Changes in ED visits and fatality rates for cardiovascular and cerebrovascular disease during the COVID-19 pandemic relative to the control period.ED visit change: 200 × ED visit of 2020/(ED visit of 2018 + ED visit of 2019)-100.Change in deaths number: 200 × Deaths number of 2020/(Deaths number of 2018 + Deaths number of 2019) -100.AHS = acute hemorrhagic stroke, AIS = acute ischemic stroke, AMI = acute myocardial infarction, COVID-19 = coronavirus disease, ED = emergency department.

Table 1
Comparison between before and during the COVID-19 pandemic.= acute hemorrhagic stroke, AIS = acute ischemic stroke, AMI = acute myocardial infarction, COVID-19 = coronavirus disease, ED = emergency department, EMS = emergency medical service.*All other regions except Seoul, Gyonggido, Incheon, Daegu, and Gyeongsangbukdo in Korea.†It includes "direct visit" and "outpatient referral."‡It includes public vehicles such as police cars, air transfers, other vehicles, and walking.§It includes hospitalizations in various wards except the ICU.www.md-journal.com AHS